Phosphorylation of Trihelix Transcriptional Repressor ASR3 by MAP KINASE4 Negatively Regulates Arabidopsis Immunity

Abstract

Proper control of immune-related gene expression is crucial for the host to launch an effective defense response. Perception of microbe-associated molecular patterns (MAMPs) induces rapid and profound transcriptional reprogramming via unclear mechanisms. Here, we show that ASR3 (ARABIDOPSIS SH4-RELATED3) functions as a transcriptional repressor and plays a negative role in regulating pattern-triggered immunity (PTI) in Arabidopsis thaliana. ASR3 belongs to a plant-specific trihelix transcription factor family for which functional studies are lacking. MAMP treatments induce rapid phosphorylation of ASR3 at threonine 189 via MPK4, a mitogen-activated protein kinase that negatively regulates PTI responses downstream of multiple MAMP receptors. ASR3 possesses transcriptional repressor activity via its ERF-associated amphiphilic repression motifs and negatively regulates a large subset of flg22-induced genes. Phosphorylation of ASR3 by MPK4 enhances its DNA binding activity to suppress gene expression. Importantly, the asr3 mutant shows enhanced disease resistance to virulent bacterial pathogen infection, whereas transgenic plants overexpressing the wild-type or phospho-mimetic form of ASR3 exhibit compromised PTI responses. Our studies reveal a function of the trihelix transcription factors in plant innate immunity and provide evidence that ASR3 functions as a transcriptional repressor regulated by MAMP-activated MPK4 to fine-tune plant immune gene expression.

Transcriptional Dynamics Driving MAMP-Triggered Immunity and Pathogen Effector-Mediated Immunosuppression in Arabidopsis Leaves Following Infection with Pseudomonas syringae pv tomato DC3000

“…Gene ontologies highlighted ABA biosynthesis as one of the earliest processes induced by effector activity, in agreement with our previous studies (de Torres-Zabala et al, 2007;de Torres Zabala et al, 2009). In parallel, transcriptional regulators were overrepresented among early DC3000-induced genes, consistent with an active suppression of MTI transcription responses (Li et al, 2015) and reflected by overrepresentation of ontologies associated with autophagy (Patel and Dinesh-Kumar, 2008) and TF import into the nucleus coincident with initial bacterial multiplication ;8 hpi. Three genes were identified as having a high number of downstream targets among genes upregulated in DC3000 response while being downregulated in DC3000hrpA-response.…”

“…The modeling predicts three TFs, XND1, FBH3, and the bZIP AT2G40620 are at the apex of a transcriptional cascade regulating a number of the TFs that collaborate to suppress host defenses. A future challenge is to identify the specific TFs directly posttranslationally modified by effectors (Li et al, 2015) that initiate the transcriptional cascade including how effector induced chromatin changes remodel the nature of the genomic landscape to facilitate the transcriptional reprogramming by early effector induced TFs to permit disease progression.…”

From Chaos to Harmony: Responses and Signaling upon Microbial Pattern Recognition

“…Specific transcription factors directly phosphorylated by MAPKs or acting downstream of Ca 2+ signaling have been shown to play a role in regulating MAMP-responsive gene expression. The Arabidopsis transcription factors ERF104 and BES1 phosphorylated by MPK6 play positive roles in MAMP-responsive gene expression (10, 70), whereas the trihelix transcription factor ASR3 phosphorylated by MPK4 negatively regulates expression of a subset of MAMP-responsive genes (81). In other cases, transcription factors are not the direct targets of MAPKs, but instead their activation is monitored by MAPK phosphorylation substrates.…”

Transcriptional Regulation of Pattern-Triggered Immunity in Plants

“…The Arabidopsis trihelix transcription factor ASR3 functions as a negative regulator in plant PTI signaling and is rapidly phosphorylated upon flg22 or elf18 treatment by the MAMP-activated MEKK1-MKK1/MKK2-MPK4 cascade (Li et al, 2015). MPK4-mediated phosphorylation of ASR3 enhances its DNA binding activity but seems not to affect its transcriptional repressor activity.…”